Long-Term Observations from Antarctica Demonstrate That

www.nature.com/scientificreports OPEN Long-term observations from Antarctica demonstrate that mismatched scales of fsheries management and predator-prey interaction lead to erroneous conclusions about precaution George M. Watters *, Jeferson T. Hinke & Christian S. Reiss Low catch limits for forage species are often considered to be precautionary measures that can help conserve marine predators. Difculties measuring the impacts of fsheries removals on dependent predators maintain this perspective, but consideration of the spatio-temporal scales over which forage species, their predators, and fsheries interact can aid assessment of whether low catch limits are as precautionary as presumed. Antarctic krill are targeted by the largest fshery in the Southern Ocean and are key forage for numerous predators. Current krill removals are considered precautionary and have not been previously observed to afect krill-dependent predators, like penguins. Using a hierarchical model and 30+ years of monitoring data, we show that expected penguin performance was reduced when local harvest rates of krill were ≥0.1, and this efect was similar in magnitude to that of poor environmental conditions. With continued climate warming and high local harvest rates, future observations of penguin performance are predicted to be below the long-term mean with a probability of 0.77. Catch limits that are considered precautionary for forage species simply because the limit is a small proportion of the species’ standing biomass may not be precautionary for their predators. To conserve large fshes, seabirds, and marine mammals, many stakeholders advocate precautionary management of fsheries that target forage species (e.g., krill, anchovies, and sardines). One strategy to conserve predators is to reserve some proportion of their prey1, perhaps by establishing a low catch limit for the fsheries that target the forage populations or stocks2. However, fshing activities may concentrate where target species are proftably caught, potentially increasing local harvest rates above intended levels3. If management fails to prevent concentrated fshing where dependent predators forage, these predators may be impacted despite a low overall catch limit. From an ecosystem perspective, the level of precaution implied by a low catch limit may be better-assessed relative to the time and space scales over which forage species, their predators, and fsheries interact. Assessing whether catch limits are precautionary from an ecosystem perspective is challenging because the impacts of forage-fsh fsheries on predators are difcult to measure4–6. Tis difculty arises because predators respond to many drivers, including environmental conditions and food-web interactions that are modulated by competition and responses to the availability of alternative prey. Reducing uncertainty to draw unambiguous inference about fsheries impacts on predators requires data that disentangle the efects of fshing from those of the environment and match the temporal and spatial scales of predator life histories, predator-prey interactions, and fshery catches. Data of this nature may not be available at the broad scale of the forage stock, but may be so on smaller scales. Experimental approaches to estimate the efects of fshing are possible7, but such experiments are rare and can be controversial8. An alternative to experimentation is to leverage long-term observational data that capture natural and anthropogenic variations in the focal system. Such long-term studies in locations where Antarctic Ecosystem Research Division, Southwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, La Jolla, California, 92037, USA. *email: [email protected] SCIENTIFIC REPORTS | (2020) 10:2314 | https://doi.org/10.1038/s41598-020-59223-9 1 www.nature.com/scientificreports/ www.nature.com/scientificreports the foraging ranges of predators overlap in time and space with locally intense fshing operations are also rare, but the observations provided by these studies may include contrasts that are sufcient to improve inference about the impacts of forage-fsh fsheries on dependent predators. Te Antarctic marine ecosystem provides a useful case study for assessing whether a catch limit established at a regional scale is precautionary given locally high harvest rates. Around the Antarctic Peninsula (AP), Antarctic krill (Euphausia superba) are the target of the largest fshery in the Southern Ocean9 and a key forage species for fshes, seabirds, and marine mammals10. Te current catch limit for krill in the entire southwest Atlantic sector of the Southern Ocean is 620,000 tons3. Tis catch limit is spatially divided across four statistical subareas (48.1, 48.2, 48.3 and 48.4; defned by the Commission for the Conservation of Antarctic Marine Living Resources) to reduce the risks of negative impacts on krill-dependent predators in the region. Te catch limit in Subarea 48.1, which surrounds the AP, is 155,000 tons, representing <1% of the estimated standing stock of krill (60.3 Mt) in the four subareas3. Te catch limit in Subarea 48.1 is achieved regularly, and catches are more concentrated in space and time than ever before9. Adélie (Pygoscelis adeliae), chinstrap (P. antarcticus), and gentoo (P. papua) penguins that breed around the AP feed on a mixed assemblage of krill, fsh, and other invertebrates11, but krill are the predom- inant prey of these seabirds12,13. In recent decades, the standing biomass of krill near the AP has varied by two orders of magnitude due to variations in the physical and biological environment14–17. Te production of penguin populations around the AP is assumed to be linked to the availability of krill18, but previous attempts to relate penguin performance with changes in krill biomass have either been unsuccessful18,19 or based on broad generali- zations inferred from trends in penguin recruitment and abundance20,21. Te low regional catch limit for krill and the lack of a quantitative relationship between krill biomass and penguin performance around the AP have been used to support arguments that current management of the krill fshery is precautionary3. We suggest, however, that the concentration of krill catches, in time and space, acts to locally increase the vulnerability of penguins to the indirect impacts of fshing despite the low regional catch limit. We investigated the efects of krill fshing on penguins near the AP consistent with best-practices5. Briefy, we compiled time-series data on 20 indices of penguin performance (e.g., foraging-trip duration, post-hatch breeding success, relative cohort strength, fedging mass) at two feld sites in the South Shetland Islands20 and on krill biomass22 in the Bransfeld Strait and the northern strata of an established survey grid23 (hereafer the Drake Passage stratum). We used the Oceanic Niño Index (ONI) and the Southern Annular Mode (SAM) as proxy indices of environmental conditions that respectively afect penguins24 and krill25. We used recent tracking data26 to match, in time and space, the penguin-performance indices with the estimates of local (stratum-specifc) krill biomass and local harvest rates (stratum-specifc krill catch divided by stratum-specifc krill biomass). We ftted a hierarchical Bayesian model to the integrated data set, frst imputing missing estimates of local krill biomass based on its relationship to the sign of the SAM during summer and then estimating the efects of the ONI, local krill biomass, and local harvest rate on penguin performance. Our integrated data characterize a highly variable ecosystem within which penguin performance has responded to fshing while some of our study populations have declined as others have increased (Fig. 1, with panels a and c respectively adapted from26 and including data from20; see Methods for further detail). Results and Discussion Variations in local krill biomass (LKB), environmental conditions, and local harvest rate (LHR) correlated with penguin performance, but variation in LKB alone had the smallest efect. To aid interpretation of our results, we defned the “best case” as conditions with ONI ≤ −0.5 °C, LKB ≤ 1 Mt, and LHR ≤ 0.01. Although it seems coun- terintuitive that the best case includes low LKB, some indices of penguin performance decrease when penguins forage on small krill20, and krill biomass is generally greatest when large cohorts of small krill recruit to the adult population16. Relative to the best case, a marginal increase in LKB (to a level >1 Mt) had the smallest efect on penguin performance (Fig. 2) and had the lowest probability (0.7) that expected performance was reduced from the best case (Table 1). Te probability that a marginal increase in LKB reduced expected penguin performance below the long-term mean performance was ≤0.04 (Table 1). Te insensitivity of penguin performance to variation in LKB corroborates previous failures to parameterize a functional response3,18,19 and seems consistent with view that krill biomass in the AP is generally sufcient to support penguin production27. Warm temperatures (ONI > −0.5 °C) and high LHR (≥0.1) decreased penguin performance, and the efects of these two factors were similar (Fig. 2). Te probabilities that the marginal efects of intermediate ONI (−0.5 °C < ONI < 0.5 °C) and high LHR caused expected performance to be less than that of the best case were ≥0.93 (Table 1). Te probabilities that these marginal efects caused expected penguin performance to be less than

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